Human Cytomegalovirus Latency and Reactivation in and Beyond the Myeloid Lineage

References

• Rook AH . Interactions of cytomegalovirus with the human immune system . Rev. Infect. Dis.10 ( Suppl. 3 ), S460 – S467 ( 1988 ).
   PubMedGoogle Scholar
• Zaia JA . The biology of human cytomegalovirus infection after bone marrow transplantation . Int. J. Cell Cloning4 ( Suppl. 1 ), 135 – 154 ( 1986 ).
   PubMedGoogle Scholar
• Orloff SL , HweeYK , KreklywichCet al. Cytomegalovirus latency promotes cardiac lymphoid neogenesis and accelerated allograft rejection in CMV naive recipients . Am. J. Transplant.11 ( 1 ), 45 – 55 ( 2012 ).
   Web of Science ®Google Scholar
• Comar M , DelbueS , LeporeLet al. Latent viral infections in young patients with inflammatory diseases treated with biological agents: prevalence of JC virus genotype 2 . J. Med. Virol.85 ( 4 ), 716 – 722 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Sissons JG , SinclairJH , BorysiewiczLK . Pathogenesis of human cytomegalovirus disease and the kidney . Kidney Int. Suppl.35 , S8 – S12 ( 1991 ).
   PubMedGoogle Scholar
• Yeager AS . Transfusion-acquired cytomegalovirus infection in newborn infants . Am. J. Dis. Child.128 ( 4 ), 478 – 483 ( 1974 ).
   PubMedGoogle Scholar
• Adler SP . Transfusion-associated cytomegalovirus infections . Rev. Infect. Dis.5 ( 6 ), 977 – 993 ( 1983 ).
   PubMedGoogle Scholar
• Tolpin MD , StewartJA , WarrenDet al. Transfusion transmission of cytomegalovirus confirmed by restriction endonuclease analysis . J. Pediatr.107 ( 6 ), 953 – 956 ( 1985 ).
   PubMed Web of Science ®Google Scholar
• Jordan MC . Latent infection and the elusive cytomegalovirus . Rev. Infect. Dis.5 ( 2 ), 205 – 215 ( 1983 ).
   PubMedGoogle Scholar
• Hansen LL , NieuwenhuisI , HoffkenG , HeiseW . [Retinitis in AIDS patients: diagnosis, follow-up and treatment] . Fortschr. Ophthalmol.86 ( 3 ), 232 – 238 ( 1989 ).
   PubMedGoogle Scholar
• Schrier RD , NelsonJA , OldstoneMB . Detection of human cytomegalovirus in peripheral blood lymphocytes in a natural infection . Science230 ( 4729 ), 1048 – 1051 ( 1985 ).
   PubMed Web of Science ®Google Scholar
• Stanier P , TaylorDL , KitchenAD , WalesN , TryhornY , TymsAS . Persistence of cytomegalovirus in mononuclear cells in peripheral blood from blood donors . BMJ299 ( 6704 ), 897 – 898 ( 1989 ).
   PubMedGoogle Scholar
• Bevan IS , DawRA , DayPJ , AlaFA , WalkerMR . Polymerase chain reaction for detection of human cytomegalovirus infection in a blood donor population . Br. J. Haematol.78 ( 1 ), 94 – 99 ( 1991 ).
   PubMed Web of Science ®Google Scholar
• Taylor-Wiedeman J , SissonsJG , BorysiewiczLK , SinclairJH . Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells . J. Gen. Virol.72 ( Pt 9 ), 2059 – 2064 ( 1991 ).
   PubMed Web of Science ®Google Scholar
• Mendelson M , MonardS , SissonsP , SinclairJ . Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors . J. Gen. Virol.77 ( Pt 12 ), 3099 – 3102 ( 1996 ).
   PubMedGoogle Scholar
• Larsson S , Soderberg-NauclerC , WangFZ , MollerE . CytomegalovirusDNA   can be detected in peripheral blood mononuclear cells from all seropositive and most seronegative healthy blood donors over time . Transfusion38 ( 3 ), 271 – 278 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Slobedman B , MocarskiES . Quantitative analysis of latent human cytomegalovirus . J. Virol.73 ( 6 ), 4806 – 4812 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Ibanez CE , SchrierR , GhazalP , WileyC , NelsonJA . Human cytomegalovirus productively infects primary differentiated macrophages . J. Virol.65 ( 12 ), 6581 – 6588 ( 1991 ).
   PubMed Web of Science ®Google Scholar
• Lathey JL , SpectorSA . Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages . J. Virol.65 , 6371 – 6375 ( 1991 ).
   PubMed Web of Science ®Google Scholar
• Soderberg-Naucler C , FishKN , NelsonJA . Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors . Cell91 ( 1 ), 119 – 126 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Reeves MB , LehnerPJ , SissonsJG , SinclairJH . An in vitro model for the regulation of human cytomegalovirus latency and reactivation in dendritic cells by chromatin remodelling . J. Gen. Virol.86 ( Pt 11 ), 2949 – 2954 ( 2005 ).
   PubMedGoogle Scholar
• Reeves MB , MacaryPA , LehnerPJ , SissonsJG , SinclairJH . Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers . Proc. Natl Acad. Sci. USA102 ( 11 ), 4140 – 4145 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Maciejewski JP , BrueningEE , DonahueRE , MocarskiES , YoungNS , St JeorSC . Infection of hematopoietic progenitor cells by human cytomegalovirus . Blood80 ( 1 ), 170 – 178 ( 1992 ).
   PubMed Web of Science ®Google Scholar
• Kondo K , KaneshimaH , MocarskiES . Human cytomegalovirus latent infection of granulocyte-macrophage progenitors . Proc. Natl Acad. Sci. USA91 ( 25 ), 11879 – 11883 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Minton EJ , TysoeC , SinclairJH , SissonsJG . Human cytomegalovirus infection of the monocyte/macrophage lineage in bone marrow . J. Virol.68 ( 6 ), 4017 – 4021 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Hahn G , JoresR , MocarskiES . Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells . Proc. Natl Acad. Sci. USA95 ( 7 ), 3937 – 3942 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Goodrum FD , JordanCT , HighK , ShenkT . Human cytomegalovirus gene expression during infection of primary hematopoietic progenitor cells: a model for latency . Proc. Natl Acad. Sci. USA99 ( 25 ), 16255 – 16260 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Hargett D , ShenkTE . Experimental human cytomegalovirus latency in CD14+ monocytes . Proc. Natl Acad. Sci. USA107 ( 46 ), 20039 – 20044 ( 2011 ).
   Web of Science ®Google Scholar
• Albright ER , KalejtaRF . Myeloblastic cell lines mimic some but not all aspects of human cytomegalovirus experimental latency defined in primary CD34+ cell populations . J. Virol.87 ( 17 ), 9802 – 9812 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Keyes LR , BegoMG , SolandM , St JeorS . Cyclophilin A is required for efficient human cytomegalovirus DNA replication and reactivation . J. Gen. Virol.93 ( Pt 4 ), 722 – 732 ( 2012 ).
   PubMedGoogle Scholar
• Penkert RR , KalejtaRF . Human embryonic stem cell lines model experimental human cytomegalovirus latency . MBio4 ( 3 ), e00298 – e00213 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Murphy EA , StreblowDN , NelsonJA , StinskiMF . The human cytomegalovirus IE86 protein can block cell cycle progression after inducing transition into the S phase of permissive cells . J. Virol.74 ( 15 ), 7108 – 7118 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Murphy Jc FW , VerdinE , SinclairJH . Control of cytomegalovirus lytic gene expression by histone acetylation . EMBO J.21 , 1112 – 1120 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Thomas MJ , SetoE . Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key?   Gene236 ( 2 ), 197 – 208 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Pizzorno MC . Nuclear cathepsin B-like protease cleaves transcription factor YY1 in differentiated cells . Biochim. Biophys. Acta1536 ( 1 ), 31 – 42 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Bain M , MendelsonM , SinclairJ . Ets-2 Repressor Factor (ERF) mediates repression of the human cytomegalovirus major immediate-early promoter in undifferentiated non-permissive cells . J. Gen. Virol.84 ( Pt 1 ), 41 – 49 ( 2003 ).
   PubMedGoogle Scholar
• Wright E , BainM , TeagueL , MurphyJ , SinclairJ . Ets-2 repressor factor recruits histone deacetylase to silence human cytomegalovirus immediate-early gene expression in non-permissive cells . J. Gen. Virol.86 ( Pt 3 ), 535 – 544 ( 2005 ).
   PubMedGoogle Scholar
• Chan G , Bivins-SmithER , SmithMS , SmithPM , YurochkoAD . Transcriptome analysis reveals human cytomegalovirus reprograms monocyte differentiation toward an M1 macrophage . J. Immunol.181 ( 1 ), 698 – 711 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Saffert RT , PenkertRR , KalejtaRF . Cellular and viral control over the initial events of human cytomegalovirus experimental latency in CD34+ cells . J. Virol.84 ( 11 ), 5594 – 5604 ( 2013 ).
   Google Scholar
• Rossetto CC , Tarrant-ElorzaM , PariGS .  Cis and trans acting factors involved in human cytomegalovirus experimental and natural latent infection of CD14 (+) monocytes and CD34 (+) cells .  PLoS Pathog.9 ( 5 ),  e1003366  ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Bolovan-Fritts CA , MocarskiES , WiedemanJA . Peripheral blood CD14(+) cells from healthy subjects carry a circular conformation of latent cytomegalovirus genome . Blood93 ( 1 ), 394 – 398 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Miyamoto T . Role of osteoclasts in regulating hematopoietic stem and progenitor cells . World J. Orthop.4 ( 4 ), 198 – 206 ( 2013 ).
   PubMedGoogle Scholar
• Tsai FY , OrkinSH . Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation . Blood89 ( 10 ), 3636 – 3643 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• De Pater E , KaimakisP , VinkCSet al. Gata2 is required for HSC generation and survival . J. Exp. Med.210 ( 13 ), 2843 – 2850 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Poole E , WaltherA , RavenK , BenedictCA , MasonGM , SinclairJ . The myeloid transcription factor GATA-2 regulates the viral UL144 gene during human cytomegalovirus latency in an isolate-specific manner . J. Virol.87 ( 8 ), 4261 – 4271 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Poole E , Mcgregor DallasSR , ColstonJ , JosephRS , SinclairJ . Virally induced changes in cellular microRNAs maintain latency of human cytomegalovirus in CD34 progenitors . J. Gen. Virol.92 ( Pt 7 ), 1539 – 1549 ( 2011 ).
   PubMedGoogle Scholar
• Reeves MB , BreidensteinA , ComptonT . Human cytomegalovirus activation of ERK and myeloid cell leukemia-1 protein correlates with survival of latently infected cells . Proc. Natl Acad. Sci. USA109 ( 2 ), 588 – 593 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Bego M , MaciejewskiJ , KhaiboullinaS , PariG , St JeorS . Characterization of an antisense transcript spanning the UL81–82 locus of human cytomegalovirus . J. Virol.79 ( 17 ), 11022 – 11034 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Goodrum F , ReevesM , SinclairJ , HighK , ShenkT . Human cytomegalovirus sequences expressed in latently infected individuals promote a latent infection in vitro . Blood110 ( 3 ), 937 – 945 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Jenkins C , AbendrothA , SlobedmanB . A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection . J. Virol.78 ( 3 ), 1440 – 1447 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Cheung AK , GottliebDJ , PlachterBet al. The role of the human cytomegalovirus UL111A gene in down-regulating CD4+ T-cell recognition of latently infected cells: implications for virus elimination during latency . Blood114 ( 19 ), 4128 – 4137 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Keyes LR , HargettD , SolandMet al. HCMV protein LUNA is required for viral reactivation from latently infected primary CD14(+) cells . PLoS ONE7 ( 12 ), e52827 ( 2013 ).
   Web of Science ®Google Scholar
• Neote K , DigregorioD , MakJY , HorukR , SchallTJ . Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor . Cell72 ( 3 ), 415 – 425 ( 1993 ).
   PubMed Web of Science ®Google Scholar
• Benedict CA , ButrovichKD , LurainNSet al. A novel viral TNF receptor superfamily member in virulent strains of human cytomegalovirus . J. Immunol.162 , 6967 – 6970 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Cheung TC , HumphreysIR , PotterKGet al. Evolutionary divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway . Proc. Natl Acad. Sci. USA37 , 13218 – 13223 . ( 2005 ).
   Google Scholar
• Poole E , KingCA , SinclairJH , AlcamiA . The UL144 gene product of human cytomegalovirus activates NFkappaB via a TRAF6-dependent mechanism . EMBO J.25 ( 18 ), 4390 – 4399 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Reeves MB , SinclairJH . Analysis of latent viral gene expression in natural and experimental latency models of human cytomegalovirus and its correlation with histone modifications at a latent promoter . J. Gen. Virol.91 ( Pt 3 ), 599 – 604 ( 2010 ).
   PubMedGoogle Scholar
• Qin Q , PenkertRR , KalejtaRF . Heterologous viral promoters incorporated into the human cytomegalovirus genome are silenced during experimental latency . J. Virol.87 ( 17 ), 9886 – 9894 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Mason GM , PooleE , SissonsJG , WillsMR , SinclairJH . Human cytomegalovirus latency alters the cellular secretome, inducing cluster of differentiation (CD)4+ T-cell migration and suppression of effector function . Proc. Natl Acad. Sci. USA109 ( 36 ), 14538 – 14543 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Weekes MP , TanSY , PooleEet al. Latency-associated degradation of the MRP1 drug transporter during latent human cytomegalovirus infection . Science340 ( 6129 ), 199 – 202 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lui KO , ZangiL , SilvaEAet al. Driving vascular endothelial cell fate of human multipotent Isl1+ heart progenitors with VEGF modified mRNA . Cell Res.23 ( 10 ), 1172 – 1186 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Goodell MA , BroseK , ParadisG , ConnerAS , MulliganRC . Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo . J. Exp. Med.183 ( 4 ), 1797 – 1806 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Quirici N , SoligoD , CanevaL , ServidaF , BossolascoP , DeliliersGL . Differentiation and expansion of endothelial cells from human bone marrow CD133(+) cells . Br. J. Haematol.115 ( 1 ), 186 – 194 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Sinzger C , GrefteA , PlachterB , GouwAS , TheTH , JahnG . Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major targets of human cytomegalovirus infection in lung and gastrointestinal tissues . J. Gen. Virol.76 ( Pt 4 ), 741 – 750 ( 1995 ).
   PubMed Web of Science ®Google Scholar
• Jarvis MA , NelsonJA . Human cytomegalovirus persistence and latency in endothelial cells and macrophages . Curr. Opin. Microbiol.5 ( 4 ), 403 – 407 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Reeves MB , ColemanH , ChaddertonJ , GoddardM , SissonsJG , SinclairJH . Vascular endothelial and smooth muscle cells are unlikely to be major sites of latency of human cytomegalovirus in vivo . J. Gen. Virol.85 ( Pt 11 ), 3337 – 3341 ( 2004 ).
   PubMedGoogle Scholar
• Belzile JP , StarkTJ , YeoGW , SpectorDH . Human cytomegalovirus infection of human embryonic stem cell-derived primitive neural stem cells is restricted at several steps but leads to the persistence of viral DNA . J. Virol.88 ( 8 ), 4021 – 4039 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Duan YL , YeHQ , ZavalaAGet al. Maintenance of large numbers of virus genomes in human cytomegalovirus-infected T98G glioblastoma cells . J. Virol.88 ( 7 ), 3861 – 3873 ( 2014 ).
   PubMed Web of Science ®Google Scholar